Abstract
Arsenic (As) is a metalloid toxic to organisms including humans. Arsenic in rice represents a significant exposure pathway for the general population, particularly for those subsisting on rice. Arsenic transformation, namely reduction, oxidation and methylation, in soil-rice systems has fundamental impacts on its mobility and toxicity. In addition to soil chemical properties (pH, Eh, metallic oxides, organic matter), microorganisms play critical roles in As transformation and mobility in paddy soil, such as through ArsM (As(III) S-adenosylmethyltransferase) and interactions with iron oxides or organic matters. Arsenic species in paddy soil directly influence As speciation in rice grain because the methylated As species in rice are mainly derived from microbial methylation in paddy soil. This paper aims to provide an overview on the status of the knowledge and gaps on the chemical aspects of As transformation in soil-rice system in conjunction with microbial ecology and functional genes. In addition, potential pathways (manipulation of microorganisms in paddy soil and genetic engineering) to decrease total As and/or inorganic As in rice grain are proposed.
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References
National Research Council. Arsenic in Drinking Water-2001 Update. Washington DC: National Academy Press, 2001
Duker A A, Carranza E J M, Hale M. Arsenic geochemistry and health. Environ Int, 2005, 31: 631–641
Kim K W, Bang S, Zhu Y, et al. Arsenic geochemistry, transport mechanism in the soil-plant system, human and animal health issues. Environ Int, 2009, 35: 453–454
Meharg A A, Hartley-Whitaker J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol, 2002, 154: 29–43
Williams P N, Islam M R, Adomako E E, et al. Increase in rice grain arsenic for regions of Bangladesh irrigating paddies with elevated arsenic in groundwaters. Environ Sci Technol, 2006, 40: 4903–4908
Zhu Y G, Sun G X, Lei M, et al. High percentage inorganic arsenic content of mining impacted and non-impacted Chinese rice. Environ Sci Technol, 2008, 42: 5008–5013
Zhu Y G, Williams P N, Meharg A A. Exposure to inorganic arsenic from rice: A global health issue? Environ Pollut, 2008, 154: 169–171
Zhao F J, Ma J F, Meharg A A, et al. Arsenic uptake and metabolism in plants. New Phytol, 2009, 181: 777–794
Mondal D, Polya D A. Rice is a major exposure route for arsenic in Chakdaha block, Nadia district, West Bengal, India: A probabilistic risk assessment. Appl Geochem, 2008, 23: 2987–2998
Meharg A A, Williams P N, Adomako E, et al. Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol, 2009, 43: 1612–1617
Li G, Sun G X, Williams P N, et al. Inorganic arsenic in Chinese food and its cancer risk. Environ Int, 2011, 37: 1219–1225
Gilbert-Diamond D, Cottingham K L, Gruber J F, et al. Rice consumption contributes to arsenic exposure in US women. Proc Natl Acad Sci USA, 2011, 108: 20656–20660
Huang H, Jia Y, Sun G X, et al. Arsenic speciation and volatilization from flooded paddy soils amended with different organic matters. Environ Sci Technol, 2012, 46: 2163–2168
Ye J, Rensing C, Rosen B P, et al. Arsenic biomethylation by photosynthetic organisms. Trends Plant Sci, 2012, 17: 155–162
Bentley R, Chasteen T G. Microbial methylation of metalloids: Arsenic, antimony, and bismuth. Microbiol Mol Biol Rev, 2002, 66: 250–271
Takamatsu T, Aoki H, Yoshida T. Determination of arsenate, arsenite, monomethylarsonate, and dimethylarsinate in soil polluted with arsenic. Soil Sci, 1982, 133: 239–246
Van Herreweghe S, Swennena R, Vandecasteele C, et al. Solid phase speciation of arsenic by sequential extraction in standard reference materials and industrially contaminated soil samples. Environ Pollut, 2003, 122: 323–342
Lakshmipathiraj P, Narasimhan B R V, Prabhakar S, et al. Adsorption of arsenate on synthetic goethite from aqueous solutions. J Hazard Mater, 2006, 136: 281–287
Cullen W R. The toxicity of trimethylarsine: An urban myth. J Environ Monit, 2005, 7: 11–15
Mestrot A, Uroic M K, Plantevin T, et al. Quantitative and qualitative trapping of arsines deployed to assess loss of volatile arsenic from paddy soil. Environ Sci Technol, 2009, 43: 8270–8275
Beesley L, Moreno-Jiménez E, Clemente R, et al. Mobility of arsenic, cadmium and zinc in a multi-element contaminated soil profile assessed by in-situ soil pore water sampling, column leaching and sequential extraction. Environ Pollut, 2010, 158: 155–160
Goldberg S. Competitive adsorption of arsenate and arsenite on oxides and clay minerals. Soil Sci Soc Amer J, 2002, 66: 413–421
Boivin P, Favre F, Hammecker C, et al. Processes driving soil solution chemistry in a flooded rice-cropped vertisol: Analysis of long-time monitoring data. Geoderma, 2002, 110: 87–107
Gao S, Tanji K K, Scardaci S C, et al. Comparison of redox indicators in a paddy soil during rice-growing season. Soil Sci Soc Amer J, 2002, 66: 805–817
Tanji K K, Gao S, Scardaci S C, et al. Characterization redox status of paddy soils with incorporated rice straw. Geoderma, 2003, 114: 333–353
Sadiq M. Arsenic chemistry in soils: An overview of thermodynamic predictions and field observations. Water Air Soil Pollut, 1997, 93: 117–136
Takahashi Y, Minamikawa R, Hattori K H, et al. Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol, 2004, 38: 1038–1044
Arao T, Kawasaki A, Baba K, et al. Effects of water management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations in Japanese rice. Environ Sci Technol, 2009, 43: 9361–9367
Huang H, Zhu Y G, Chen Z, et al. Arsenic mobilization and speciation during iron plaque decomposition in a paddy soil. J Soils Sediments, 2012, 12: 402–410
Yamaguchi N, Nakamura T, Dong D, et al. Arsenic release from flooded paddy soils is influenced by speciation, Eh, pH, and iron dissolution. Chemosphere, 2011, 83: 925–932
Munch J C, Hillebrand T, Ottow J C G. Transformations in the Feo/Fed ratio of pedogenic iron oxides affected by iron-reducing bacteria. Can J Soil Sci, 1978, 58: 475–486
Sahrawat K L. Fertility and organic matter in submerged rice soils. Curr Sci, 2005, 88: 735–739
Yu K, Patrick W H. Redox range with minimum nitrous oxide and methane production in a rice soil under different pH. Soil Sci Soc Amer J, 2003, 67: 1952–1958
Klitzke S, Lang F. Mobilization of soluble and dispersible lead, arsenic, and antimony in a polluted, organic-rich soil — effects of pH increase and counterion valency. J Environ Qual, 2009, 38: 933–939
Wilson S C, Lockwood P V, Ashley P M, et al. The chemistry and behaviour of antimony in the soil environment with comparisons to arsenic: A critical review. Environ Pollut, 2010, 158: 1169–1181
Livesey N T, Huang P M. Adsorption of arsenate by soils and its relation to selected properties and anions. Soil Sci, 1981, 131: 88–94
Brouwere K D, Smolders E, Merckx R. Soil properties affecting solid-liquid distribution of As(V) in soils. Eur J Soil Sci, 2004, 55: 165–173
Smedley P L, Kinniburgh D G. A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem, 2002, 17: 517–568
Pedersen H D, Postma D, Jakobsen R. Release of arsenic associated with the reduction and transformation of iron oxides. Geochim Cosmochim Acta, 2006, 70: 4116–4129
Burton E D, Johnston S G, Watling K, et al. Arsenic effects and behavior in association with the Fe(II)-catalyzed transformation of schwertmannite. Environ Sci Technol, 2010, 44: 2016–2021
Clemente R, Dickinson N M, Lepp N W. Mobility of metals and metalloids in a multi-element contaminated soil 20 years after cessation of the pollution source activity. Environ Pollut, 2008, 155: 254–261
Beesley L, Dickinson N. Carbon and trace element mobility in an urban soil amended with green waste compost. J Soils Sediments, 2010, 10: 215–222
Weng L, Van Riemsdijk W H, Hiemstra T. Effects of fulvic acids on arsenate adsorption to goethite: Experiments and modelling. Environ Sci Technol, 2009, 43: 7198–7204
Williams P N, Zhang H, Davison W, et al. Organic matter-solid phase interactions are critical for predicting arsenic release and plant uptake in Bangladesh paddy soils. Environ Sci Technol, 2011, 45: 6080–6087
Marschner H. Mineral Nutrition of Higher Plants. 2nd ed. London: Academic Press, 1995
Fitz W J, Wenzel W W. Arsenic transformations in the soil-rhizophere-plant system: Fundamentals and potential application to phytoremediation. J Biotechnol, 2002, 99: 259–278
Cao X, Ma L Q, Shiralipour A. Effects of compost and phosphate amendments on arsenic mobility in soils and arsenic uptake by the hyperaccumulator Pteris vittata L. Environ Pollut, 2003, 126: 157–167
Jain A, Loeppert R H. Effect of competing ions on the adsorption of arsenate and arsenite by ferrihydrite. J Environ Qual, 2000, 29: 1422–1430
Bang S, Meng X. A review of arsenic interactions with anions and iron hydroxides. Environ Eng Res, 2004, 9: 184–192
Ma J F, Yamaji N, Mitani N, et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA, 2008, 105: 9931–9935
Li R Y, Stroud J L, Ma J F, et al. Mitigation of arsenic accumulation in rice with water management and silicon fertilization. Environ Sci Technol, 2009, 43: 3778–3783
Oremland R S, Stolz J F. The ecology of arsenic. Science, 2003, 300: 939–944
Qin J, Rosen B P, Zhang Y, et al. Arsenic detoxification and evolution of trimethylarsine gas by a microbial arsenite S-adenosylmethionine methyltransferase. Proc Natl Acad Sci USA, 2006, 103: 2075–2080
Bachate S P, Khapare R M, Kodam K M. Oxidation of arsenite by two β-proteobacteria isolated from soil. Appl Microbiol Biotechnol, 2012, 93: 2135–2145
Páez-Espino D, Tamames J, de Lorenzo V, et al. Microbial responses to environmental arsenic. Biometals, 2009, 22: 117–130
Kuehnelt D, Goessler W. Organoarsenic compounds in the terrestrial environment. In: Craig P J, ed. Organometallic Compounds in the Environment. Heidelberg: Wiley Publishers, 2003. 223–275
Yin X X, Chen J, Qin J, et al. Biotransformation and volatilization of arsenic by three photosynthetic cyanobacteria. Plant Physiol, 2011, 156: 1631–1638
Yin X X, Zhang Y Y, Yang J, et al. Rapid biotransformation of arsenic by a model protozoan Tetrahymena thermophila. Environ Pollut, 2011, 159: 837–840
Yin X X, Wang L H, Bai R, et al. Accumulation and transformation of arsenic in the blue-green alga Synechocysis sp. PCC6803. Water Air Soil Pollut, 2012, 223: 1183–1190
Shariatpanahi M, Anderson A C, Abdelghani A A, et al. Biotransformation of the pesticide sodium arsenate. J Environ Sci Health B, 1981, 16: 35–47
Michalke K, Wickenheiser E B, Mehring M, et al. Production of volatile derivatives of metal(loid)s by microflora involved in anaerobic digestion of sewage sludge. Appl Environ Microbiol, 2000, 66: 2791–2796
Wang G, Kennedy S P, Fasiludeen S, et al. Arsenic resistance in Halobacterium sp. strain NRC-1 examined by using an improved gene knockout system. J Bacteriol, 2004, 186: 3187–3194
Thomas F, Diaz-Bone R A, Wuerfel O, et al. Connection between multimetal(loid) methylation in methanoarchaea and central intermediates of methanogenesis. Appl Environ Microbiol, 2011, 77: 8669–8675
McBride B C, Wolfe R S. Biosynthesis of dimethylarsine by methanobacterium. Biochemistry, 1971, 10: 4312–4317
Liu X Z, Zhang L M, Prosser J I, et al. Abundance and community structure of sulfate reducing prokaryotes in a paddy soil of southern China under different fertilization regimes. Soil Biol Biochem, 2009, 41: 687–694
Erkel C, Kube M, Reinhardt R, et al. Genome of rice cluster I archaea—The key methane producers in the rice rhizosphere. Science, 2006, 313: 370–372
Ladha J K, Reddy P M. Nitrogen fixation in rice systems: State of knowledge and future prospects. Plant Soil, 2003, 252: 151–167
Zhang Y Y, Yang J, Yin X X, et al. Arsenate toxicity and stress responses in the freshwater ciliate Tetrahymena pyriformis. Eur J Protistol, 2012, 48: 227–236
Bhattacharjee H, Rosen B P. Arsenic metabolism in prokaryotic and eukaryotic microbes. In: Nies D H, Silver S, eds. Molecular Microbiology of Heavy Metals. Heidelberg: Springer-Verlag Publishers, 2007. 371–406
Rensing C, Rosen B. Heavy Metals Cycles (arsenic, mercury, selenium, others). Encyclopedia of Microbiology. UK: Elsevier Press, 2009
Huysmans K D, Frankenberger W T. Evolution of trimethylarsine by a Penicillium sp. isolated from agricultural evaporation pond water. Sci Total Environ, 1991, 105: 13–28
Mladenov N, Zheng Y, Miller M P, et al. Dissolved organic matter sources and consequences for iron and arsenic mobilization in Bangladesh aquifers. Environ Sci Technol, 2010, 44: 123–128
Li H J, Peng J J, Karrie A W, et al. Phylogenetic diversity of Fe(III)-reducing microorganisms in rice paddy soil: Enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sediments, 2011, 11: 1234–1242
Kögel-Knabner I, Amelung W, Cao Z, et al. Biogeochemistry of paddy soils. Geoderma, 2010, 157: 1–14
Wang X J, Yang J, Chen X P, et al. Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. J Soils Sediments, 2009, 9: 568–577
Wang Z S, Chen X P, Wang X J, et al. The effect of anaerobic redox cycling of iron on arsenic mobility in paddy (in Chinese). Asian J Ecotoxicol, 2010, 5: 862–867
Chen X P, Zhu Y G, Hong M N, et al. Effects of different forms of nitrogen fertilizers on arsenic uptake by rice plants. Environ Toxicol Chem, 2008, 27: 881–887
Chen C C, Dixon J B, Turner F T. Iron coatings on rice roots: morphology and models of development. Soil Sci Soc Amer J, 1980, 44: 1113–1119
Chen Z, Zhu Y G, Liu W J, et al. Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol, 2005, 165: 91–97
Liu W J, Zhu Y G, Smith F A, et al. Do phosphorus nutrition and iron plaque alter arsenate (As) uptake by rice seedlings in hydroponic culture? New Phytol, 2004, 162: 481–488
Liu W J, Zhu Y G, Hu Y, et al. Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L). Environ Sci Technol, 2006, 40: 5730–5736
Yang J, Hu Y, Wang X J, et al. Differences of iron plaque formation and As accumulation between two rice cultivars with different aerenchyma tissue (in Chinese). Asian J Ecotoxicol, 2009, 4: 711–717
Wu C, Ye Z, Shu W, et al. Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes. J Exp Bot, 2011, 62: 2889–2898
Liu W J, Zhu Y G, Smith F A. Effects of iron and manganese plaques on arsenic uptake by rice seedlings (Oryza sativa L.) grown in solution culture supplied with arsenate and arsenite. Plant Soil, 2005, 277: 127–138
Inskeep W P, Macur R E, Hamamura N, et al. Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol, 2007, 9: 934–943
Bhattacharya P, Welch A H, Stollenwerk K G, et al. Arsenic in the environment: Biology and chemistry. Sci Total Environ, 2007, 379: 109–120
Weiss J V, Emerson D, Megonigal J P. Geochemical control of microbial Fe(III) reduction potential in wetlands: Comparison of the rhizosphere to non-rhizosphere soil. Fems Microbiol Ecol, 2004, 48: 89–100
Weiss J V, Emerson D, Backer S M, et al. Enumeration of Fe (II)-oxidizing and Fe (III)-reducing bacteria in the root zone of wetland plants: Implications for a rhizosphere iron cycle. Biogeochemistry, 2003, 64: 77–96
Slobodkin A I, Jeanthon C, L’Haridon S, et al. Dissimilatory reduction of Fe(III) by thermophilic bacteria and archaea in deep subsurface petroleum reservoirs of western siberia. Curr Microbiol, 1999, 39: 99–102
Lovley D R, Holmes D E, Nevin K P. Dissimilatory Fe(III) and Mn(IV) reduction. Advan Microb Physiol, 2004, 49: 219–286
Weber K A, Achenbach L A, Coates J D. Microorganisms pumping iron: Anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol, 2006, 4: 752–764
Hori T, Müller A, Igarashi Y, et al. Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J, 2010, 4: 267–278
Hajiboland R, Aliasgharzad N, Barzeghar R. Phosphorus mobilization and uptake in mycorrhizal rice (Oryza sativa L.) plants under flooded and non-flooded conditions. Acta Agr Slov, 2009, 93: 153–161
Li H, Ye Z H, Chan W F, et al. Can arbuscular mycorrhizal fungi improve grain yield, As uptake and tolerance of rice grown under aerobic conditions? Environ Pollut, 2011, 159: 2537–2545
Li H, Wu C, Ye Z H, et al. Uptake kinetics of different arsenic species in lowland and upland rice colonized with Glomus intraradices. J Hazard Mater, 2011, 194: 414–421
Wang X J, Chen X P, Yang J, et al. Effect of microbial mediated iron plaque reduction on arsenic mobility in paddy soil. J Environ Sci-China, 2009, 21: 1562–1568
Arao T, Kawasaki A, Baba K, et al. Effects of arsenic compound amendment on arsenic speciation in rice grain. Environ Sci Technol, 2011, 45: 1291–1297
Lomax C, Liu W J, Wu L, et al. Methylated arsenic species in plants originate from soil microorganisms. New Phytol, 2011, 193: 665–672
Raab A, Williams P N, Meharg A, et al. Uptake and translocation of inorganic and methylated arsenic species by plants. Environ Chem, 2007, 4: 197–203
Carey A M, Scheckel K G, Lombi E, et al. Grain unloading of arsenic species in rice (Oryza sativa L.). Plant Physiol, 2010, 152: 309–319
Zheng M Z, Cai C, Hu Y, et al. Spatial distribution of arsenic and temporal variation of its concentration in rice. New Phytol, 2011, 189: 200–209
Carey A M, Norton G J, Deacon C, et al. Phloem transport of arsenic species from flag leaf to grain during grain filling. New Phytol, 2011, 192: 87–98
Mestrot A, Feldmann J, Krupp E M, et al. Field fluxes and speciation of arsines emanating from soils. Environ Sci Technol, 2011, 45: 1798–1804
Mestrot A, Merle J K, Broglia A, et al. Atmospheric stability of arsine and methylarsines. Environ Sci Technol, 2011, 45: 4010–4015
Meng X Y, Qin J, Wang L H, et al. Arsenic biotransformation and volatilization in transgenic rice. New Phytol, 2011, 191: 49–56
Zhu Y G, Rosen B P. Perspectives for genetic engineering for the phytoremediation of arsenic contaminated environments: From imagination to reality? Curr Opin Biotechnol, 2009, 20: 220–224
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Zheng, R., Sun, G. & Zhu, Y. Effects of microbial processes on the fate of arsenic in paddy soil. Chin. Sci. Bull. 58, 186–193 (2013). https://doi.org/10.1007/s11434-012-5489-0
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DOI: https://doi.org/10.1007/s11434-012-5489-0